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Age and Ageing Advance Access published September 25, 2014

Age and Ageing 2014; 0: 112


doi: 10.1093/ageing/afu115

The Author 2014. Published by Oxford University Press on behalf of the British Geriatrics Society.
This is an Open Access article distributed under the terms of the Creative Commons Attribution
License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution,
and reproduction in any medium, provided the original work is properly cited.

SYSTEMATIC REVIEW

Prevalence of and interventions for sarcopenia in


ageing adults: a systematic review. Report of the
International Sarcopenia Initiative (EWGSOP
and IWGS)

Servicio de Geriatra, Hospital Universitario Ramn y Cajal, Ctra. Colmenar km 9, 1, 28034 Madrid, Spain
Istituto di Medicina Interna e Geriatria, Universit Cattolica del Sacro Cuore, Rome, Italy
3
Gastroentrologie et Nutrition Clinique, CHU de Nice, Universit de Nice Sophia-Antipolis, Nice, France
4
Universidad Autonoma de Baja California, Tijuana Baja California Mexico, Mexico
5
Department of Human Health Sciences, Kyoto University, Graduate School of Medicine, Kyoto, Japan
6
Unit de Nutrition Humaine, UMR 1019, INRA, Universit Clermont-Ferrand, CHU de Clermont-Ferrand, France
7
Center for Geriatrics and Gerontology, Taipei Veterans General Hospital, Taipei, Taiwan
8
Nutrition, Exercise Physiology, and Sarcopenia Laboratory, Jean Mayer Human Nutrition Research Center on Aging at Tufts
University, Boston, MA, USA
9
Department of Ageing and Health, Guys and St Thomas NHS Foundation Trust, London, UK
10
Dpartement de Rhabilitation et Griatrie, Hpitaux Universitaires de Genve-Suisse, Geneva, Switzerland
11
Institut for Biomedicine of Ageing, University Erlangen-Nrnberg, Erlangen, Germany
12
Institute for Exercise Physiology and Wellness Research, University of Central Florida, Orlando, FL, USA
13
Division of Geriatric Medicine, University of Pittsburgh, Pittsburgh, PA, USA
14
Department of Geriatric Medicine, Inserm U558 Le Centre Hospitalier Universitaire de Toulouse (CHU) Grontople,
Toulouse, France
15
Department of Medicine and Therapeutics, Prince of Wales, Hospital, Chinese University of Hong Kong, Hong Kong SAR,
The Peoples Republic of China
16
Division of Geriatrics, Department of Medicine, University of Verona, Verona, Italy
17
Department of Public Health and Caring Sciences/Clinical Nutrition and Metabolism, Uppsala University, Uppsala, Sweden
2

Address correspondence to: A. J. Cruz-Jentoft. Tel: +34 913368172, Email: ajcruzjentoft@telefonica.net

Abstract
Objective: to examine the clinical evidence reporting the prevalence of sarcopenia and the effect of nutrition and exercise
interventions from studies using the consensus denition of sarcopenia proposed by the European Working Group on
Sarcopenia in Older People (EWGSOP).
Methods: PubMed and Dialog databases were searched ( January 2000October 2013) using pre-dened search terms.
Prevalence studies and intervention studies investigating muscle mass plus strength or function outcome measures using the
EWGSOP denition of sarcopenia, in well-dened populations of adults aged 50 years were selected.
Results: prevalence of sarcopenia was, with regional and age-related variations, 129% in community-dwelling populations, 14
33% in long-term care populations and 10% in the only acute hospital-care population examined. Moderate quality evidence suggests that exercise interventions improve muscle strength and physical performance. The results of nutrition interventions are
equivocal due to the low number of studies and heterogeneous study design. Essential amino acid (EAA) supplements, including

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ALFONSO J. CRUZ-JENTOFT1, FRANCESCO LANDI2, STPHANE M. SCHNEIDER3, CLEMENTE ZIGA4,


HIDENORI ARAI5, YVES BOIRIE6, LIANG-KUNG CHEN7, ROGER A. FIELDING8, FINBARR C. MARTIN9, JEANPIERRE MICHEL10, CORNEL SIEBER11, JEFFREY R. STOUT12, STEPHANIE A. STUDENSKI13, BRUNO VELLAS14, JEAN WOO15,
MAURO ZAMBONI16, TOMMY CEDERHOLM17

A. J. Cruz-Jentoft et al.
2.5 g of leucine, and -hydroxy -methylbutyric acid (HMB) supplements, show some effects in improving muscle mass and
function parameters. Protein supplements have not shown consistent benets on muscle mass and function.
Conclusion: prevalence of sarcopenia is substantial in most geriatric settings. Well-designed, standardised studies evaluating exercise or nutrition interventions are needed before treatment guidelines can be developed. Physicians should screen for sarcopenia in
both community and geriatric settings, with diagnosis based on muscle mass and function. Supervised resistance exercise is recommended for individuals with sarcopenia. EAA (with leucine) and HMB may improve muscle outcomes.
Keywords: exercise intervention, nutrition intervention, prevalence, age-related, sarcopenia, older people

Methods

Although exercise and nutrition interventions have proved


efcacy to treat different conditions in various populations
of adults and older people, the effects in those with sarcopenia have received less attention. Sarcopenia has been dened
as the loss of skeletal muscle mass and strength that occurs
with advancing age [1]. However, until recently, there has
been no widely accepted denition of sarcopenia that was
suitable for use in research and clinical practice.
A practical clinical denition of, and consensus diagnostic
criteria for, age-related sarcopenia was developed in 200910
and reported by the European Working Group on Sarcopenia
in Older People (EWGSOP) [2]. The EWGSOP provided a
working denition of sarcopenia as a syndrome characterised
by progressive and generalised loss of skeletal muscle mass
and strength with a risk of adverse outcomes such as physical
disability, poor quality of life and death [2]. They proposed
that sarcopenia is diagnosed using the criteria of low muscle
mass and low muscle function (either low strength and/or low
physical performance) [2]. A similar approach was taken in
2009 by the International Working Group on Sarcopenia
(IWGS), who provided a consensus denition of sarcopenia
as age-associated loss of skeletal muscle mass and function.
This group proposed that sarcopenia is diagnosed based on a
low whole-body or appendicular fat-free mass in combination
with poor physical functioning [3].
To date, most prevalence and intervention studies have
used varied denitions of sarcopenia that are not current
(e.g. based only on decreased muscle mass) and the results
may therefore be misleading and difcult to interpret.
However, with the implementation of new operational denitions of sarcopenia, it may be possible to dene the natural
course of the condition and determine which treatments are
effective. In 2013, representatives of the EWGSOP, IWGS
and international experts from Asia and America came together to form the International Sarcopenia Initiative (ISI)
with the intention of developing a systematic review of some
aspects of sarcopenia. Specically, the aims of this systematic
review were to (i) assess the prevalence of sarcopenia using
denitions that include both muscle mass and muscle function, as proposed by the EWGSOP and the IWGS; and
(ii) to review interventions with nutrition and exercise that
used both muscle mass and muscle function as outcomes.

Search strategy

PubMed and Dialog databases were searched from January


2000 to May 2013 using the pre-dened search terms sarcopenia and muscle mass: additional pre-dened search terms
were applied (see Supplementary data available in Age and
Ageing online, Appendix S1) for each of the three areas of
interest: prevalence of sarcopenia, nutrition interventions
for sarcopenia and exercise interventions for sarcopenia
(Figure 1). An additional short search of PubMed and Dialog
databases using the terms sarcopenia, elderly, intervention,
prevalence and treatment was conducted to cover articles
published in the period MayOctober 2013 (Figure 1). The
reference lists of systematic review articles and meta-analyses
were scanned for any additional references missed from the
PubMed and Dialog searches. The expert group was also
asked to identify and provide any additional papers; they
deemed to have been missed in the formal literature searches.

Eligibility criteria

Across all three categories, only studies that enrolled participants aged 50 years and older within well-dened populations (such as those in community-dwelling, hospital and
nursing home/geriatric settings) were included. Prevalence
studies were included if sarcopenia had been assessed
according to the EWGSOP denition of sarcopenia, i.e.
based on muscle mass and muscle strength or physical performance [2]. They were excluded if they only used muscle
mass to dene sarcopenia. Nutrition and exercise intervention studies were included if the outcome measures reported
for the interventions included muscle mass and at least one
measure of muscle strength or physical performance, even
when the population studied was not dened as sarcopenic.
If these outcomes were not clearly stated within the study
methodology, the study was excluded. Other criteria used
to exclude studies in each of the three categories are provided
in Supplementary data available in Age and Ageing online,
Appendix S2.
Observational studies were included in the prevalence category, but for the exercise and nutrition intervention categories,
only randomised controlled trials were selected. The ISI group

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Introduction

Prevalence of and interventions for sarcopenia in ageing adults

was divided into three subgroups (prevalence, exercise and nutrition). Final papers selected for inclusion in each of the three
categories were agreed upon by each subgroup consensus.

supplementation improve measures of muscle mass, muscle


strength, and physical performance? Based on the answers to
these questions, draft recommendations were proposed by
the co-chairs, and the working group then reviewed these
recommendations to reach a consensus.

Data synthesis

Data tables were compiled independently for each topic. For


the prevalence of sarcopenia category, data were recorded on
demographics (country, gender and age), assessment method
used for each domain (muscle mass, muscle strength and
physical performance) and sarcopenia prevalence. For the
interventional categories, data were collected on population,
numbers studied (by gender), age, intervention, control
group, duration of intervention, outcomes measured and the
main results. The methodological quality of each randomised,
controlled trial was assessed using the 11-point Physiotherapy
Evidence Database (PEDro) scale. Each item on the scale
that the trial satised (except for item 1, which assesses external validity and is not included in the total score) contributed
one point to the total PEDro score, with 0 representing the
lowest score and 10 the highest [4]. This scale was specically
developed to rate the quality of randomised, controlled trials
evaluating physical therapist interventions.
The following questions were investigated in patients aged
50 years and older without comorbid conditions. What is the
prevalence of sarcopenia in different populations? Is physical
exercise (as physical activity, resistance training or endurance
training) effective compared with control in improving measures of muscle loss, muscle mass, muscle strength and physical performance? Compared with control, does nutrition

Results
Overall, 4810 publications were identied (Figure 1). Of
these, 3909 were excluded, leaving 901 publications for potential inclusion ( prevalence: 252; exercise: 175; nutrition:
474). In addition, 11 papers were identied as suitable for inclusion as a result of a short search of PubMed and Dialog
databases to identify articles published in the period May
October 2013.
Eighteen prevalence, 7 exercise and 12 nutrition papers
were nally chosen by the working group members for inclusion within this review (Figure 1).
Estimates of prevalence

Of the 18 prevalence studies meeting the inclusion criteria,


15 (83%) were in community-dwelling patients [5, 69, 10,
11, 12, 13, 14, 15, 16, 17, 18, 19], with two studies in patients
in long-term care institutions [20, 21], and one publication in
the acute hospital-care setting [22] (Table 1). The reporting
of age varied across studies, but for those where the mean
age was given, this ranged from 59.2 to 85.8 years [5, 69, 10,
11, 12, 13, 14, 16, 17, 18, 19, 21].

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Figure 1. Selection of papers.

Reference

Date data collected

Country

M/F, n

Assessment method
Muscle mass

Muscle strength

Physical
performance

Age, years Mean


(SD) [Range]

Sarcopenia prevalence, %
Total

Male

Female

.................................................................................................................
Community-dwelling populations
Abellan van Kan et al. [5]
Jan 1992Jan 1994

France

0/3025

DEXA

HS

GS

80.51 (3.9)
[75]
82.2 (1.4)
[8085]
85.8 (4.9)
73.7 (5.6)

5.2

5.2

21.8

25.7

19.8

29.1
7.8a
16.6b
12.5

27.1
10.8a
14.9b
14.6

30.1
3.7a
19.0b
12.4

4.1

S: 5
SS: 0

S: 7
SS: 0

(A): 6.8
(B): 7.8

4.6

7.9

0.9

0.9

24.2

24.2

11.3

10.7

S: 3.7
SS: 0
10.2

2.6

6.7

21.8

22.1

All: 14.3
5064: 12.7
65: 17.4

Landi et al. [6]

Oct 2003

Italy

66/131

MAMC

HS

GS

Landi et al. [7]


Lee et al. [8]

Oct 2003

Italy
Taiwan

118/236
223/163

MAMC
DXA

HS
HS, KE, PEF

Legrand et al. [9]

Nov 2008Sep 2009

Belgium

103/185

BIA

HS

GS
SPPB, GS, TUG,
or SCPT
mSPPB, GS

Malmstrom et al. [10]

Sep 2000Jul 2001

124/195

DEXA

GS

McIntosh et al. [11]

USA (African
Americans)
Canada

84.8 (3.6)
[>80]
59.2 (4.4)

42/43

BIA

HS

GS

75.2 (5.7)

6.0

Murphy et al. [12]

USA

1426/1502

DEXA

HS

GS

S: 5

Patel et al. [13]

UKc

Cohort A: 103/0
Cohort B: 765/1022

DEXA, SFT

HS

GS, TUG,
chair-rise time

Patil et al. [14]

Finland

0/409

DEXA

HS

GS, SPPB, TUG

Sanada et al. [15]

Japan

0/533

DEXA

HS, LEP

Sit and reach,


VO2max

Tanimoto et al. [16]

MayJun 2007,
2008, 2009

Japan

364/794

BIA

HS

GS

Verschueren et al. [17]

Belgium, UK

679/0

DEXA

HS, KE

GS

Volpato et al. [18]

20042006

Italy

250/288

BIA

HS

GS

Yamada et al. [19]

Japan

568/1314

BIA

HS

GS

F: 73.5 (2.88)
M: 73.8 (2.85)
Total: [7079]
(A): 72.5 (2.5)
(B): M, 67.0 (2.6);
F, 67.1 (2.6)
74.2 (3.0)
[7080]
<39: 11.4%
<49: 21.2%
<59: 25.9%
<69: 29.8%
<85: 11.6%
[3084]
M: 74.4 (6.4)
F: 73.9 (6.3)
[65]
59.6 (10.7)
[4079]
77.1 (5.5)
[6597]
74.9 (5.5)
[6589]

Institutional dwelling
Bastiaanse et al. [20]

Netherlands

450/434

CC

HS

GS

5059: 46.5%
6069: 35.2%
7079: 16.2%
80: 2.1%
[50]

A. J. Cruz-Jentoft et al.

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Table 1. Prevalence of sarcopenia

ALM, appendicular lean mass; BIA, bioelectrical impedance analysis; CC, calf circumference; DEXA, dual-energy X-ray absorptiometry; F, female; GS, gait speed; HS, hand-grip strength using a dynamometer; KE, knee
extensor; LEP, leg extension power; M, male; MAMC, mid-arm muscle circumference; PEF, peak expiratory flow; S, sarcopenia; SCPT, stair-climb power test; SD, standard deviation; SFT, skin-fold thickness; (m)SPPB,
(modified) standard physical performance battery; SS, severe sarcopenia; TUG, timed-up-and-go; VO2max, maximal oxygen uptake.
a
By relative appendicular skeletal muscle index.
b
By percentage skeletal muscle index.
c
Consists of two cohorts (Cohort A: detailed data were collected. Cohort B: same data were collected, but no DEXA).
*P < 0.001 versus females.

10.2
[65]

MAMC
UK
Acute hospital care
Gariballa and Alessa [22]

227/205

HS

84.1 (4.8)
[70]
HS
BIA
31/91
Italy
AugSep 2010
Landi et al. [21]

The prevalence of EWGSOP-dened sarcopenia was


129% (up to 30% in women) for older adults living in the
community [5, 69, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19],
1433% (up to 68% in men) for those living in long-term
care institutions [20, 21] and 10% for those in acute hospital
care [22]. Age was not consistently reported across the
studies, with some giving mean ages only, others reporting
ranges, and others breaking age down into categories; thus, a
comprehensive analysis of prevalence based on age could not
be made. However, where reported, the majority of studies
suggested the prevalence of sarcopenia increased with age
[18, 19, 22]. However, one study appeared to show a decrease
in sarcopenia prevalence with increasing age [20]. In one
study, sarcopenia appeared to be related to gender, with
males more commonly affected than females [21], while
another study showed a numerically higher prevalence of sarcopenia and severe sarcopenia in women than in men [13]. In
a further study, the prevalence of sarcopenia was higher in
women than in men in those aged <75 years; but, in those
aged >85 years, the prevalence of sarcopenia was higher in
men than in women (P < 0.05) [19]. However, in most
studies that reported gender, there was no signicant association with sarcopenia prevalence [69, 11, 16, 19, 20].
Exercise interventions

There were seven moderate quality (PEDro score: 46) intervention studies that investigated the effect of exercise on
muscle parameters in different populations aged 6095 years
(Table 2) [2329]. The impact of exercise on sarcopenia was
assessed using muscle mass and muscle strength or power
measures in all studies [2329]; assessment of physical performance (chair rise [24], 12-min walk [25], stair climbing
[29] or timed up and go [27, 28]) was carried out in ve of
seven studies (Table 2).
Resistance training interventions

Resistance training was explored in four mixed-gender studies


(Table 2) [2325, 29]. When used from 318 months, resistance training interventions alone improved muscle mass in
two of four studies [23, 29] and muscle strength in three of
four studies [23, 25, 29] compared with control (low-intensity
home exercise or standard rehabilitation). Physical performance (chair rise, stair climb or 12-min walk) improved with
resistance training alone versus control in all three studies
assessing this parameter [24, 25, 29].
Combined exercise/physical activity interventions

Three additional studies explored compound exercise interventions (with different blends of aerobic, resistance, exibility and/or balance training), which were performed for 318
months [2628]. A high-intensity multipurpose exercise programme over 18 months improved muscle mass, muscle
strength and physical performance versus control (wellbeing)
in a study in 246 women [27]. In two mixed-gender studies

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GS

32.8

67.7

20.8*

Prevalence of and interventions for sarcopenia in ageing adults

Reference

Population

Number
studied
(M/F)

Age, years
Mean (SD)
[Range]

91

83 (4)

Progressive RET; CON


(low-intensity home exercise)

MM (DEXA), MS (KE)

57 (7/50)

83

98 (36/62)

70

RET + SUPP; CON + SUPP;


RET + PLA; PLA + CON
RET + SUPP; SUPP; RET; CON

18

MM (FFM by labelled water),


MP, PP (chair rise)
MM (DEXA), MS (quadriceps
strength), PP (12-min walk)

Intervention
Description

Duration
(months)

PEDro
score

Outcomes measured

Main results

.................................................................................................................
Binder et al.
[23]

Frail, community-dwelling

Bonnefoy et al. Frail, care institution


[24]
Bunout et al.
Community-dwelling
[25]

Suetta et al.
[29]

Frail, post-operative
36 (18/18)
elective hip replacement

[6086]

RET; ES; CON (standard


rehabilitation)

MM (US), MS (quadriceps), PP
(stair climbing)

Goodpaster
et al. [26]

Sedentary,
community-dwelling

42 (11/31)

[7089]

PA (aerobic, strength, flexibility,


balance training); CON (health
education)

12

MM (CT scan), MS (KE)

Kemmler et al. Community-dwelling


[27]

246 (0/246)

69.1 [6580]

High-intensity multipurpose exercise


programme; CON (wellbeing)

18

MM (DEXA), MS (isometric
leg extension), PP (timed up
and go)

Rydwik et al.
[28]

96 (38/58)

>75

PA (aerobic, muscle strength, balance


exercises); nutrition intervention;
PA + nutrition intervention; CON

MM [FFM = BW-fat mass (skin


folds)], MS (leg press, dips),
PP (timed up and go)

Frail, community-dwelling

Total body FFM increased in the progressive


RET group, but not in the CON group
(P = 0.005)
MS increased to a greater extent in the
progressive RET than in the CON group
(P = 0.05)
RET did not improve MM or MP, but
improved PP versus CON (P = 0.01)
FFM did not change in any group
RET improved MS versus CON (P < 0.01)
PP remained constant in RET group, but
declined in the CON group (P < 0.01).
RET improved MM, MS and PP versus CON
(all P < 0.05)
In the ES or CON groups, there was no
increase in any measurement outcomes
MM decreased in both groups (but losses
were not different between groups)
MS loss was decreased in CON, but
completely prevented in PA (between group
change not significant)
Multipurpose exercise was associated with
significant improvements in MM
(P = 0.008), MS (P = 0.001), PP (P < 0.001)
versus CON
PA improved MS (P < 0.01 for dips), but did
not improve MM or PP versus CON

BW, body weight; CON, control; CT, computerised tomography; DEXA, dual-energy X-ray absorptiometry; ES, electrical stimulation; F, female; FFM, free-fat mass; FM, fat mass; KE, knee extension; M, male; min, minute;
MM, muscle mass; MP, muscle power; MS, muscle strength; RET, resistance exercise training; PA, physical activity; PLA, placebo; PP, physical performance; SD, standard deviation; SUPP, nutritional supplement;
US, ultrasound.

A. J. Cruz-Jentoft et al.

6
Table 2. Summary of the effect of exercise on sarcopenia in randomised, controlled studies meeting the inclusion criteria

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Prevalence of and interventions for sarcopenia in ageing adults


[26, 28], muscle mass did not improve; muscle strength
(assessed as dips) improved with physical activity versus
control at 3-months follow-up in one of the two studies [28];
and physical performance did not improve in the one study
in which it was assessed [28].
Overall, most exercise trials showed improved muscle
strength and physical performance (using different measures),
but only three of seven studies found increased muscle mass.
These trials were largely performed in community-dwelling
older people, sometimes identied as frail by different
measures.

duration each, in community-dwelling individuals. Daily


leucine amount provided was 2.8 and 2.5 g. EAA improved
muscle mass in one of two studies [33], did not improve
muscle strength, and improved physical performance in the
study that used this outcome [35]. When combined with exercise, EAA improved leg muscle mass and muscle strength
but not physical performance versus health education at
3 months [35].
Overall, very limited evidence on EAA supplementation
seems to show some effects on muscle mass and function.
HMB supplementation

Nutrition interventions

The effect of HMB alone [32, 36] or HMB in combination


with ARG and LYS [34] or resistance exercise training [39]
on muscle parameters has been investigated in four highquality (PEDro score: 810) studies of 824-week duration
in community-dwelling older adults [34, 36, 39] or in healthy
older adults on extended bed rest [32]. HMB prevented
muscle mass loss in one of four studies and did not improve
muscle mass in the other three [32]; improved muscle strength
in one [34] (and possibly two) [36] of four studies and
improved physical performance in one of four studies [34].
Overall, HMB showed some effects on muscle mass and
function in these high-quality studies, but sample sizes were
small.
Fatty acids

Protein supplements

Protein supplementation (with other nutrients providing


400 extra kilocalories/day in three of ve studies) either
alone or in addition to resistance exercise training was evaluated in ve moderate- to high-quality (PEDro score: 410)
studies [24, 25, 30, 37, 38]. In the only high-quality study with
no associated exercise in a frail, community-dwelling population, protein supplementation improved physical performance, but not muscle mass or muscle strength versus control
[38]. Only in one of the four moderate- to high-quality
studies using different types and amounts of protein supplementation in addition to an exercise programme for 24
weeks to 18 months [24, 25, 30, 37], was muscle mass
increased over the control group [40]. Muscle strength did
not change in any of the studies; only a transient increase in
muscle power was found in one study [24]. Physical performance did not improve in any of these four studies.
Overall, these ve moderate- to high-quality studies fail to
show a consistent effect of protein supplementation on
muscle mass and function [24, 25, 30, 37, 38].

Essential amino acid supplementation

The effect of essential amino acid (EAA) supplementation


either alone [33] or in combination with resistance exercise
training [35] on muscle parameters was investigated in two
high-quality (PEDro score: 7 and 8) studies of 3 months

The only study examining the effect of fatty acid supplementation (-linolenic acid) on muscle parameters (PEDro score:
10), in 51 older adults undergoing resistance training for 12
weeks, showed no effect of the supplementation on muscle
mass or muscle strength versus placebo [31].

Discussion
Sarcopenia is an independent risk factor for adverse outcomes, including difculties in instrumental and basic ADL
[6, 10, 16, 20, 21], osteoporosis [17], falls [21], hospital length
of stay and re-admission [22] and death [6]. This underscores
the importance of understanding the true prevalence of sarcopenia and effective preventative strategies.
Prevalence

The prevalence of sarcopenia in the literature varies widely,


and is likely to be affected by the population studied (including the population under investigation and the reference population) and the different methods used to assess
muscle mass, muscle strength and physical performance
[3]; although results may also be due to real differences in
prevalence of sarcopenia. As studies that dened sarcopenia
as muscle mass plus muscle strength/physical performance
were few, comparisons of prevalence across studies were
difcult due to the different methods and cut-off points

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Most studies (11/12) evaluating nutrition intervention in


adults aged 50 years and over (Table 3) were in communitydwelling populations whose age ranged from 62 to 90 years
(n = 1498) [25, 3039]. One study assessed individuals
living in care institutions (mean age, 83 years; n = 57) [24].
Nutrition interventions that were identied included protein
supplementation (usually with other nutrients providing
extra calories) [24, 25, 30, 37, 38], amino acid (mainly leucine)
supplementation [33, 35], -hydroxy -methylbutyric acid
(HMB; a bioactive metabolite of leucine) supplementation
with arginine [34] or alone [32, 34, 36, 39] or fatty acid supplementation [31] administered over 836 weeks to evaluate
changes in muscle mass and/or strength and function.

Reference

Population

Number studied
(M/F)

Age, years, mean


(SD) [range]

PEDro
Score

Intervention (duration)

Outcomes measured

Main results

.................................................................................................................
Bonnefoy et al. [24]

Frail, care institution

57 (7/50)

83

RET + SUPP (400 kcal, 30 g of


protein/day); CON + SUPP;
RET + PLA;
PLA + CON (9 months)

Bunout et al. [25]

Community-dwelling

98 (36/62)

[70]

RET + SUPP (400 kcal, 13 g of


protein/day); SUPP; RET; CON
(18 months)

Chale et al. [30]

Sedentary,
community-dwelling

80 (33/47)

[7085]

10

Tieland et al. [37]

Frail,
community-dwelling

62 (21/41)

10

Tieland et al. [38]

Frail,
community-dwelling

65 (29/36)

Dillon et al. [33]

Healthy individuals

14 (0/14)

Kim et al. [35]

Community-dwelling

155 (0/155)

PLA: 79 (6)
Protein: 78 (9)
[65]
PLA: 81 (1 SEM)
Protein 78 (1
SEM)
65
All: 68 (2)
PLA: 69 (3)
Supplement: 67 (1)
79 (2.9)
[75]

WPS (378 kcal, 40 g of protein/


day) + RET; CON (378 kcal, no
protein) + RET (6 months)
Protein (30 g/day) + RET;
PLA + RET (24 weeks)

Flakoll et al. [34]

Community-dwelling

57 (0/57)

Deutz et al. [32]

Healthy individuals on
bed rest

19 (4/15)

MM (FFM by labelled water), MP, SUPP significantly increased MP at 3


PP (chair rise, 6-min walk, stair
months versus CON (P = 0.03), but
climb)
not at 9 months
SUPP did not improve MM or PP
versus CON
MM (DEXA), MS (biceps and
SUPP alone had no effect on MM, MS
quadriceps strength), PP
or PP
(12-min walk)
SUPP did not show an additive effect
over RET outcome
MM (DEXA, CT scan), MS (KE), WPS + RET did not improve MM, MS
PPPP (stair climb, chair rise,
or PP significantly versus
400 m walk, SPPB)
CON + RET
MM (DEXA), MS (leg press,
Protein + RET significantly improved
LE, HS), PP (SPPB)
MM (P = 0.006), but not MS or PP
versus PLA + RET
MM (DEXA), MS (leg press,
PP improved significantly with protein
LE, HS), PP (SPPB)
supplementation (P = 0.02), but not
MM or MS versus PLA

Protein (30 g/day); PLA; (24 weeks)

EAA (HIS, ILE, LEU, LYS, MET,


PHE, THR, VAL); PLA; (3 months)

MM (DEXA), MS (bicep curl,


triceps extension, LE, leg curl)

EAA (LEU, LYS, VAL, ILE, THR,


PHE) + RET; EAA; RET; HE
(3 months)

MM (BIA), MS (KE), PP (max.


walking speed)

76.7
[6290]

ARG + HMB + LYS; PLA (12 weeks)

MM (BIA), MS (isometric leg


strength, HS), PP
(get up and go)

PLA: 67.1 (1.7)


HMB: 67.4 (1.4)
[6076]

10

HMB; PLA
Bed rest (10 days) + rehabilitation
(8 weeks)

MM (DEXA), MS (KE, leg


press), PP (SPPB, get up and
go, 5-item PPB)

EAA increased MM versus baseline,


(P < 0.05)
There were no changes in MS
EAA alone improved PP, but not MM
and MS versus HE
EAA + RET improved leg (not
appendicular or total) MM
(P < 0.007) and, MS (P = 0.02)
versus HE
PP was not more improved by the
addition of EAA than by RET alone
MS (P 0.05) and PP (P = 0.002)
significantly improved with
ARG + HMB + LYS versus PLA
ARG + HMB + LYS did not
significantly improve MM versus
PLA
Bed rest caused a significant decrease in
MM (P = 0.02) in the PLA group,
but MM was preserved in the HMB
group
Changes in MS and PP were not
significant for HMB versus PLA

A. J. Cruz-Jentoft et al.

8
Table 3. Summary of the effect of nutrition on sarcopenia in randomised, controlled studies meeting the inclusion criteria

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ALA, -linolenic acid; ARG, arginine; BIA, bioelectrical impedance analysis; CON, controls; CT, computerised tomography; DEXA, dual X-ray absorptiometry; EAA, essential amino acid; F, female; FFM, fat-free mass; HE,
health education; HIS, histidine; HMB, -hydroxy -methylbutyrate; ILE, isoleucine; HS, hand-grip strength; KE, knee extension; LE, leg extension; LEU, leucine; LYS, lysine; M, male; min, minute; MET, methionine; MM,
muscle mass; MP, muscle power; MS, muscle strength; NS, not significant; PHE, phenylalanine; PLA, placebo; PP, physical performance; RET, resistance exercise training; SD, standard deviation; SPPB, standard physical
performance battery; SUPP, nutritional supplement; THR, threonine; VAL, valine; WPS, whey protein supplement.

ALA + RET; PLA + RET (12 weeks)


10
65.4 (0.8)
51 (28/23)
Community-dwelling
Cornish and
Chilibeck [31]

70 (1)
Community-dwelling
Vukovich et al. [39]

31 (15/16)

10

HMB + RET; PLA + RET (8 weeks)

MM (DEXA), MS (isokinetic
leg strength, HS), PP
(get up and go)
Phase I: HMB; PLA (24 weeks)
Phase II: PLA + RET; HMB + RET
(24 weeks)
9
73 (1 SEM)
[65]
98 (49/49)
Community-dwelling
Stout et al. [36]

used. The prevalence of sarcopenia in the community using


a denition consistent with EWGSOP was 133% across
different populations (male and female data combined),
with higher prevalence, as expected, in settings where older,
more complex or acutely ill individuals are cared for.
Ethnicity may also play a role, especially if the reference and
study populations do not match.
After careful consideration of the methodological limitations and scope of these studies, the ISI group proposes
certain recommendations for the design of future studies
(expert advice):
Studies with sufcient sample size to identify prevalence
and risk factors for sarcopenia, including subpopulation
analyses, are needed.
Studies should focus on standardised, well-dened, reproducible populations, namely community-dwelling individuals, individuals living in nursing homes/care homes, and
acutely ill or physically frail inpatients. These populations
should be clearly described so that studies can be compared
for external validity.
Standardised models and cut-off points should be used for
each domain of the denition of sarcopenia to allow comparison between studies.
Longitudinal studies on the incidence of sarcopenia are
needed, again using standard methods.

Exercise intervention

Exercise interventions appear to have a role in increasing


muscle strength and improving physical performance, although they do not seem to consistently increase muscle
mass, in frail, sedentary, community-dwelling older individuals. Investigations in other populations are still anecdotal.
No trials were found that recruited individuals based on their
sarcopenic status. The results suggested that combining
various types of exercise into a programme may also improve
muscle strength and physical performance. Most exercise
studies involved limited participants and were mainly conducted within a single country.
Recommendations for the design of exercise studies
(expert advice):
Improved standardisation of exercise interventions is
needed, to allow for replication and contrast.
Studies should have common outcome measures, along
with similar time points for assessment (e.g. 4 weeks, 8
weeks, 3 months, 6 months, 1 year), so that valid comparisons across studies can be made. The short physical performance battery, gait speed, 400-m walking distance and
grip strength are proposed as useful measures of physical
performance that are able to determine clinically signicant
changes. Grip strength, chair rise and knee extension may
be used to measure muscle strength.
Exercise interventions should focus on well-dened populations, with well-dened sarcopenia.

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HMB alone significantly improved


some, but not all measures of MS
versus PLA. No significant changes
were found in MM and PP with
HMB versus PLA
Adding HMB to RET did not improve
any parameters over RET alone
MM (DEXA, CT scan), MS (misc. MM improved with HMB + RET
upper and lower body strength
versus PLA + RET, but not
press, flexion and extension
significantly (P = 0.08)
measurements)
MS did not improve with HMB + RET
versus PLA + RET
MM (DEXA, US), MS
ALA + RET had minimal effect on
(leg press, chest press)
MM or MS versus PLA + RET

Prevalence of and interventions for sarcopenia in ageing adults

A. J. Cruz-Jentoft et al.
Nutrition intervention

Recommendations for the design of nutrition studies


(expert advice)

Further studies are needed to determine the effect of different nutrition interventions on muscle mass and function
using robust, multi-centre and standardised approaches
with single or complex nutrition interventions and clinically
relevant outcomes (muscle strength, physical performance).
Studies using four arms (exercise, nutrition, both or none)
should also be conducted. The choice of exercise and nutrition interventions should be based on the singular effect of
each intervention.
Outcome measures for such studies should not differ from
those used for individual components, and reporting
should allow for individual group comparisons to also
evaluate the role of each component.
Timing of nutrition intervention before or after exercise
should be explored in clinical trials comparing different times
of administration, as basic studies suggest there may be timeassociated differences in the effect of nutrition intervention
over exercise.
Baseline nutritional status and physical frailty of the population should be considered when doing nutrition intervention studies.

Key points
The reported prevalence of sarcopenia in the community is
up to 33%, with higher prevalence in long-term and acute
care settings.
This underscores the importance of preventative and clinical
management strategies for managing sarcopenia.
While further research is needed on interventions, we
provide recommendations for clinical practice.
The ISI included representatives of the European Working
Group on Sarcopenia in Older People (EWGSOP), the
International Working Group on Sarcopenia (IWGS) and
international experts.

Practice recommendations

Sarcopenia is a common clinical problem in people over 50


years of age, and one that leads to severe adverse outcomes.
Research on management interventions is advancing quickly,
but questions still remain. Based on our current understanding, the expert group agreed some general recommendations
for clinical practice (expert opinion):
(1) Sarcopenia, dened as low muscle mass and low muscle
function and/or reduced physical performance, occurs in

10

Conflicts of interest
Abbott had no role in the choice of members of the group,
but had the right to have an observer member at the meetings. Members of the Working Group received no salary or
other incomes from the European Union Geriatric medicine
Society (EUGMS), Abbott Nutrition (AN) or any other

Downloaded from http://ageing.oxfordjournals.org/ by guest on October 10, 2014

Although nutrition intervention is considered one of the mainstays of intervention in sarcopenia, much of the evidence is
based on short-term protein synthesis studies, and large clinical
trials are still lacking. Our review has failed to show a consistent
effect of protein supplementation, although the number of
studies found using our strict selection criteria was very low.
EAAs (with 2.5 g of leucine) and HMB seem to have some
effects on muscle mass and muscle function that need to be
conrmed in larger trials. Vitamin D studies were evaluated as
part of the review process; while some epidemiological studies
link vitamin D levels with muscle parameters, there were no
intervention studies meeting the criteria for inclusion in this
review. Similarly, there is a large literature on the effects of
omega 3-fatty acids on muscle parameters, especially in cachexia,
but only one negative study was found in this review [31].
Interventions that evaluated the combined effects of exercise
and nutrition sometimes suggested a potential additive effect, although this needs further research. However, solid evidence on
which to base recommendations for patients with sarcopenia is
not available.

at least 1 in 20 community-dwelling individuals, and


prevalence may be as high as 1 in 3 in frail older people
living in nursing homes (Table 1).
Owing to the consequences of sarcopenia on quality
of life, disability and mortality, it is recommended that
physicians should consider screening for sarcopenia,
both in community and geriatric settings.
The new denitions of sarcopenia, based on muscle
mass and function, should be preferred to denitions
based on muscle mass alone.
(2) Exercise interventions, especially those based on resistance training, may have a role in improving muscle
strength and physical performance (moderate quality evidence), but not muscle mass. Moreover, exercise has
been shown to improve other common conditions in
adults and older patients, as well as being safe.
Supervised resistance exercise or composite exercise
programmes may be recommended for frail or sedentary community-dwelling individuals.
Time of intervention of at least 3 months and probably
longer may be needed to obtain signicant improvement
in relevant clinical parameters (muscle strength and
physical performance). Increased physical activity in
daily life may also be recommended in these individuals.
(3) Some nutrition interventions such as EAAs (with 2.5 g
of leucine) and HMB may improve muscle parameters.
Although our ndings did not appear to support this approach, increasing protein intake to 1.2 g/kg body
weight/day, either by improving diet or adding protein
supplements, has been recommended for adults and
older people by an expert group [40]. Evidence to recommend specic interventions is yet to be established.

Prevalence of and interventions for sarcopenia in ageing adults


organisation for any of the tasks involved in the preparation
of this manuscript or for attending the meetings of the
group. An individual COI form has been lled by each
member of the International Sarcopenia Initiative group.
Medical writing support was provided by Mike Musialowski
at Lucid with funding from AN.

Funding
This work was supported by an unrestricted educational
grant provided by AN to EUGMS. This grant was used for
operational activities including two meetings of the Working
Group.

Supplementary data

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Received 22 January 2014; accepted in revised form 25 June
2014

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